Plant disease management in organic farming systems

Review Received: 21 June 2015 Revised: 7 August 2015 Accepted article published: 1 September 2015 Published online in Wiley Online Library: 6 October 2015 (wileyonlinelibrary.com) DOI 10.1002/ps.4145 Plant disease management in organic farming systems Ariena HC van Bruggen,a* Abraham Gamlielb and Maria R Finckhc Abstract Organic farming (OF) has significantly increased in importance in recent decades. Disease management in OF is largely based on the maintenance of biological diversity and soil health by balanced crop rotations, including nitrogen-fixing and cover crops, intercrops, additions of manure and compost and reductions in soil tillage. Most soil-borne diseases are naturally suppressed, while foliar diseases can sometimes be problematic. Only when a severe disease outbreak is expected are pesticides used that are approved for OF. A detailed overview is given of cultural and biological control measures. Attention is also given to regulated pesticides. We conclude that a systems approach to disease management is required, and that interdisciplinary research is needed to solve lingering disease problems, especially for OF in the tropics. Some of the organic regulations are in need of revision in close collaboration with various stakeholders. © 2015 Society of Chemical Industry Keywords: organic agriculture; plant diseases; cultural control; biological control; soil health; systems approach 1 INTRODUCTION 30 Organic farming (OF) can be defined as ‘an ecologically, economically and socially responsible way of farming, providing an enduring supply of safe and healthy food and fibers, with the least possible losses of nutrients and energy, and the least negative impacts on the environment, as regulated by certification agencies’.1,2 Worldwide, OF has increased tremendously in importance over the past 20 years, including in developing countries, and the global market for organic products reached a value of almost $US 72 billion in 2013.3 OF is governed by the idea that all natural processes within an agroecosystem are mutually dependent on each other, and that management should aim at achieving and supporting self-regulation through natural processes.4 This has been laid down in detail in the OF standards as formulated by the International Federation of Organic Agricultural Movements (IFOAM) (http://www.ifoam.org/about_ifoam/standards/index.html). Thus, solutions to problems are primarily sought within the ecological possibilities of the farming system. Cropping systems based on monocropping of genetically uniform varieties and high external inputs, typical of conventional farming (CF), have favored epidemic development of many plant diseases caused by fungi, bacteria, nematodes and viruses (van Bruggen AHC et al., accepted for publication).5 – 8 The degradation of soil structure and soil quality by loss of soil organic matter favors root diseases. Soil fumigation creates a biologically impoverished, substrate-rich environment favoring the explosive development of plant pathogens that happen to (re)enter the fumigated soil. In addition, high concentrations of nitrogen and imbalances in plant nutrition lead to greater susceptibility to a variety of root and foliar pathogens.9 The relation between root disease suppression and a large number of soil health characteristics has been reviewed in detail.8 Compared with CF, OF systems generally have: (i) higher plant diversity in time and space; (ii) rotations and cover cropping, Pest Manag Sci 2016; 72: 30–44 which lead to a higher soil organic matter content; (iii) a higher biomass, diversity and activity of soil microorganisms and fauna; (iv) an increase in water holding capacity, reduced run-off and increased rooting depth, leading to enhanced water use efficiency; (v) improved cation exchange capacity, increased internal cycling and reduced loss of nutrients.10 – 12 These intrinsic differences between OF and CF systems have resulted in differences in the occurrence and intensity of plant diseases and pests, but these are reviewed elsewhere and will not be discussed in this review.8,13 In this review, we describe the various disease management options in OF that can also be useful for other farmers and researchers who strive for greater ecological sustainability. We discuss the practices used to manage disease development and conclude with some suggestions for research on plant disease management in OF. 2 PLANT DISEASE MANAGEMENT IN ORGANIC AGRICULTURE Pest and disease control in OF is to a large extent based on the maintenance of soil fertility by balanced crop rotations, including nitrogen-fixing crops, winter cover crops, intercrops, additions of manure and compost and reductions in soil tillage.14 – 16 ∗ Correspondence to: Ariena HC van Bruggen, Department of Plant Pathology and Emerging Pathogens Institute, University of Florida, Gainesville, FL 32611, USA. E-mail: ahcvanbruggen@ufl.edu a Department of Plant Pathology and Emerging Pathogens Institute, University of Florida, Gainesville, FL, USA b Agriculture Research Organization, ARO Volcani Center , Bet Dagan, Israel c Faculty of Organic Agricultural Sciences, Ecological Plant Protection, University of Kassel, Witzenhausen, Germany www.soci.org © 2015 Society of Chemical Industry Plant disease management in organic farming systems www.soci.org Table 1. General control tactics and specific measures used at different stages of pathogen invasion in organic in comparison with conventional crop production7,13,15,96 Invasion stage/general approach Colonization prevention Sanitation Temporal asynchrony Non-conducive conditions Synthetic chemical barrier Spatial isolation Prevent landing Population regulation Host plant resistance Intercropping Competition and antagonism Unsuitable environment Specific practices Pathogen-free seed, debris destruction, flaming; steaming Late or early planting/harvest with respect to pathogen or vector arrivals Crop rotation; repellent cultivars; enhanced soil suppressiveness by organic amendments, biochar; calcium carbonate, dolomitic lime, gypsum Preventive foliar sprays with synthetic insecticides, nematicides, acaricides, fungicides or bactericides; botanical pesticides containing petroleum derivatives Crops sown distant from pest/pathogen hosts, weeds, non-crop hosts removed; barrier crops or natural strips Vector trapping, reflective mulches, oil sprays Frequency in organic in comparison with conventional crop production Similarly common; rare More common Longer rotation; similar cultivars; more organic amendments; similar non-synthetic inorganic amendments Absent Occasional; barriers and natural strips more common Similarly occasional Suboptimal plant quality (low fertilization), classical genetic resistance, crop spacing Mixed cultivars, mixed cropping, strip cropping, green manures Enhanced microbial activity and diversity to reduce pathogen populations (compost, chitin, compost teas, plant extracts, humates, microbial products as spray or seed treatment) Ventilation, humidity and temperature control (greenhouses), humidity control by irrigation More common Various systemic and contact insecticides and fungicides; synthetic pyrethroids Soaps, oils, compost teas, acetic acid Sulfur dust and sprays, diatomaceous earth, micronutrients (Si or Zn); copper sulfate, copper hydroxide, bordeaux mixture, potassium phosphite, potassium bicarbonate, potassium silicate Plant extracts without petroleum-based synergists (pyrethrum, nicotine, neem, horsetail, seaweed, yucca) Parasitoids (e.g. parasitic wasps), bacteria (e.g. Bacillus thuringiensis, B. subtilis, Pseudomonas), fungi (e.g. Trichoderma) Trapping, vacuuming, handpicking Absent; exceptional More common More common Similarly common Curatives after establishmenta Synthetic pesticides Organics Inorganics Botanicals Inundative biological control Physical removal More common More common; in some countries Rare or common Occasional (no petroleum-based synergists or carriers) Occasional, similar to CF a In the plant pathology literature, only systemic fungicides with kickback action are considered to be curative, but here we include any pesticides that limit further spread of pests and diseases in the plant population. Pest Manag Sci 2016; 72: 30–44 manure will lead to a microbially driven system and changes in micronutrient supplies. This can greatly affect plant resistance and the pathogen-beneficial microbial balance in the soil.9,22,23 Four basic tactics for disease management will be discussed: (1) preventing pathogen introduction by preplant measures; (2) limiting pathogen entry by minimizing initial inoculum; (3) regulation of pathogen establishment by minimizing the suitability of the host and its environment for infection and reproduction; (4) pathogen control by employing curative methods that limit further spread. 2.1 Preplant measures When soil-borne diseases and pests are threatening plant establishment and survival, elimination of the pathogens and pests can be attempted by sanitation and soil disinfestation. Soil disinfestation will change the soil ecosystem with the aim of reducing a broad spectrum of fungi, bacteria, nematodes and weeds. © 2015 Society of Chemical Industry wileyonlinelibrary.com/journal/ps 31 Crop rotations are generally longer and spatial diversity is greater under organic compared with conventional management.17 Crop sequences are adjusted to optimize nutrient availability and minimize the risk of weeds, diseases and pests.18,19 Increased habitat diversity is also used to enhance natural pest and disease control, among others by intercropping and planting of trees, shrubs, wild grasses and flowering plants (Table 1).6,11 – 13 Genetically modified organisms (GMOs) are not used, partly because of concerns about the unknown impacts of gene manipulation, but also to avoid genetic uniformity, which can promote pest and disease outbreaks.2,6 Thus, crop protection in OF is not directed at controlling possible pathogens directly, but at management of the environment such that plants are able to withstand potential attacks.13 Organic growers commonly rely on cultural plant protection methods.7,20,21 Substitution of synthetic fertilizers by organic amendments and www.soci.org Several methods of soil disinfestation can be used in OF as long as chemical pesticides are not involved, namely flooding, soil steaming, solarization, biological soil disinfestation and biofumigation. Flooding is rarely used owing to lack of water in most areas. Soil steaming is used occasionally for organic greenhouse production, but this method actually goes against the production principles of many organic growers because it creates a biological vacuum in the soil.24 Therefore, flooding and steaming will not be discussed any further. Sanitation is an essential preplant measure to reduce the initial inoculum of a wide array of plant pathogens. For example, the initial inoculum of Venturia inaequalis, the causal agent of apple scab, is reduced by winter pruning or by enhancing the breakdown of apple leaves after adding an N-rich organic fertilizer (such as a byproduct of the sugar industry, vinasse) in fall and winter.25 In organic greenhouse production, crop residues with overwintering inoculum are commonly removed. The residues are often composted, and care has to be taken to attain sufficiently high temperatures by regular turning of the composting materials to kill residual pathogens.2 Weed control is especially important to minimize the potential spread of virus diseases. In vineyards and orchards, diseased branches are commonly pruned away and again composted or (less frequently) burned.26,27 In organic fields, crop stubble is treasured and will never be burned to prevent loss of organic carbon in the form of CO2 . Better alternatives to burning are shallow incorporation of the debris to provide substrate to the soil food web, or leaving it on the surface for slower decomposition to prevent erosion. In spite of the lack of removal of infected stubble, diseases may be controlled owing to greater soil health. For example, eyespot (Pseudocercosporella herpotrichoides) and footrot (Fusarium sp.) of wheat were less prevalent on a low-input farm with shallow tillage than on a neighboring conventional farm with deeper tillage, and sharp eyespot (Rhizoctonia cerealis) was initially increased but later suppressed after several years of minimum till.7,28 This last disease practically disappeared in a long-term experiment with organic fertilization in the Pacific North West.29 Cull piles of diseased crops must be avoided, however. This is especially true for potatoes with late blight, caused by Phytophthora infestans.30 Covering or removal of cull piles and removal of volunteer potatoes and alternative hosts are even more important for organic than for conventional farmers to manage late blight, as other control options are limited in OF. 32 2.1.1 Soil solarization Soil solarization consists of covering moist soil with a layer of transparent plastic, exposed to sunlight during a few weeks in the summer. Sheets of clear, UV-stable polyethylene-based plastic are stretched across the field and glued together at their joints.31 Under a single layer of plastic, temperatures of 45–50 ∘ C can be reached to a depth of 10–15 cm and temperatures of 40–45 ∘ C to a depth of 15–30 cm in the field, but under a double plastic layer (in the open field) or with a single layer inside a closed greenhouse, soil temperatures can be further elevated by an additional 5–8 ∘ C.31 The method has also been adapted to vegetable production on raised beds mulched with polyethylene outdoors, to greenhouse production and to perennial crops.32 – 35 Soil solarization affects soil-borne pathogens and pests directly through heat inactivation of cellular processes and indirectly by increasing their sensitivity to antagonistic microorganisms and abiotic stresses. It can also enhance plant growth by increasing the wileyonlinelibrary.com/journal/ps A HC van Bruggen, A Gamliel, M R Finckh Figure 1. Soil solarization applied to control broomrape for a carrot crop on an organic farm in the Bet Shean Valley, Israel, in 2014. The seams of the plastic sheets are connected by open flame welding rather than gluing (photograph by Abraham Gamliel). availability of mineral nutrients and improving soil tilth. The ultimate effectiveness of soil solarization depends on the maximum and minimum temperatures reached and the depth to which the soil is heated, as well as the sensitivity of the targeted pathogens. Root-knot and cyst nematodes are sensitive in the upper solarized soil layer (killed at 45–50 ∘ C). However, they may survive solarization in deeper soil layers (40 cm). Most plant-pathogenic fungi and bacteria are quite sensitive (45–55 ∘ C), except for heat-tolerant species (55–65 ∘ C).34,36,37 Most plant viruses are inactivated in the range 55–70 ∘ C, and most weed seeds are killed between 50 and 60 ∘ C, but again there are some exceptions.38 Soil solarization is frequently used by organic growers in Israel (Fig. 1) and Florida.31,32,39 The application of solarization requires addressing aspects of soil preparation, tarping and plastics technology, which are essential for achieving successful solarization. The need for application methodologies suited to each specific solarization niche, e.g. open field, closed greenhouse and strip or bed solarization, has led to specialized equipment, such as plastic films with better soil heating capacity.31,39 Furthermore, the technologies for laying the plastic and anchoring it to the soil have been improved significantly by using specific machinery, special glues and other methods of plastic welding.31,39 Special care is taken to recycle the plastic. 2.1.2 Biological or anaerobic soil disinfestation Anaerobic soil disinfestation (ASD) involves the incorporation of fresh organic material in moist soil under airtight plastic for 3–6 weeks, depending on the outside temperature.40,41 The carbon source provides a substrate for the proliferation of bacteria, which deplete the available oxygen, so that anaerobic bacteria continue to decompose the carbon source as long as the oxygen remains sufficiently low. Strong to moderate anaerobic conditions, as measured by an oxygen probe (around 1% oxygen in the soil air) or an oxidative reduction potential meter (between −300 and −200 mV), are required during the treatment period. ASD is often used by vegetable growers in the Netherlands, on strawberry beds in California and in greenhouses in Japan.32,40,41 ASD is effective at controlling several soil-borne plantpathogenic fungi, bacteria and nematodes, including Fusarium oxysporum, Rhizoctonia solani, R. tuliparum, Sclerotinia sclerotiorum, Verticillium dahlia, Ralstonia solanacearum, Globodera rostochiensis, Pratylenchus spp. and Meloidogyne spp.40,42 – 44 Moreover, the growth of most weeds is also drastically reduced © 2015 Society of Chemical Industry Pest Manag Sci 2016; 72: 30–44 Plant disease management in organic farming systems after ASD treatment. ASD is not only effective for the production of healthy annual crops but also in perennial orchards.43 The method has been adapted for raised beds in Florida and California; the plastic serves as mulch after the ASD treatment.32 The levels of pathogen reduction are similar to those obtained using chemical soil disinfestations against soil-borne pathogens and pests. In addition, more nitrogen is available after ASD. Together, these effects generally result in improved crop growth. The exact modes of action of ASD are still uncertain. The creation of anaerobic conditions in the soil leads to the accumulation of toxic products, including alcohols, aldehydes, organic acids and other volatile compounds, as well as a low pH, which can all affect the survival of soil-borne pathogens.41,45 In addition to the toxic products produced, biocontrol by anaerobic bacteria such as Bacillus and Clostridium spp. may contribute to pathogen inactivation. A shift in the microbial community composition has been demonstrated, while the microbial diversity is unaffected.44 ASD induces microbial changes in the soil that are relatively persistent.44 These often result in general disease suppression that can remain active for several years.42 Pest Manag Sci 2016; 72: 30–44 namely neutral pH, moderate temperature and high soil moisture content, are important.49 Better results are observed in light soil relatively low in organic matter than in heavy soils rich in organic matter, where movement of volatiles may be reduced. Incorporation of plant materials can also affect disease control through alternative mechanisms besides their production of biotoxic volatile compounds, for example by microbial activation and changes in microbial community structure.55,56 The method has been optimized and frequently used in Australia, and is now also implemented in Israel and China.49,55 The effectiveness of biofumigant green manures can be improved by combining them with soil heating.54,57 For example, the combination of solarization and chicken compost reduced both root-knot nematode galls and Pythium on lettuce compared with the effect of solarization alone.58 However, the implementation of solarization combined with the incorporation of organic amendments involves adjustments in the cropping system, including rotation of the appropriate crops. 2.2 Limiting pathogen entry in organic crops Practices preventing entry by pathogens, namely the use of clean seeds or vegetative propagating materials, crop rotation, spatial isolation and removal of certain weeds, hold for both OF and CF. Diseases can also be avoided by planting susceptible crops at times of the year when certain diseases or vectors are less pervasive and by taking measures to prevent virus transmission by insects. 2.2.1 Healthy seeds and planting materials Seeds and planting materials used in organic crop production must originate from certified organic sources, provided that organically produced materials are available.59,60 Officially registered seeds and vegetative material must be true to type, pure and free from plant pathogens and pests. For economic reasons associated with the limited scale of organic production, only a restricted number of organically grown cultivars are currently available. Conventional cultivars are often used, because breeding for agronomic and disease resistance characteristics suitable for OF is still in its infancy.61 Thus, diseases that are commonly controlled by fungicides on conventional seed, such as smuts and bunts of cereal crops, may become problematic when conventional, susceptible cultivars are used for organic production, where seed treatment with fungicides is not allowed.62 To promote the selection and production of well-adapted local varieties, seeds may be produced on organic crop production farms, but the health status of such seeds could be jeopardized.60,63 Organically produced seeds must be extracted from fruits by natural means such as fermentation. The addition of hydrochloric acid, which limits bacterial infections in conventionally produced seeds, is not permitted in organic seed production. Chemical seed treatment after extraction is not allowed either. There are three main seed treatment methods for organically produced seeds: (1) physical methods; (2) treatment with plant extracts; (3) seed coating with biological control agents or their extracts.64 – 66 As physical methods, hot water or steam treatment, followed by drying, can be used in organic seed production.65 Various plant extracts (ethereal oils), organic acids and biological control agents have been tested for the control of seed-borne pathogens.64,65,67,68 An emulsion of thyme oil and a solution of ascorbic acid were most promising, although these can be phytotoxic at too high concentrations and have not been registered yet for organic production.69 Several biocontrol agents are commercially available to treat organic © 2015 Society of Chemical Industry wileyonlinelibrary.com/journal/ps 33 2.1.3 Aerobic soil disinfestation – biofumigation Aerobic soil disinfestation, which is usually called ‘biofumigation’, is based on the generation of toxic volatiles in the soil by certain organic amendments. Some high nitrogen amendments, such as fish meal, blood meal and feather meal, generate ammonia which is toxic to a wide range of pathogens and nematode pests and can reduce various soil-borne diseases.46,47 In addition, volatile fatty acids can be emitted by some animal manures.47 The most common biofumigation method is the cultivation, maceration and incorporation into soil of green manure crops that contain precursors of toxic compounds. Examples of such precursors are glucosinolates, which are commonly produced in members of the Brassicaceae family, including rapeseed and mustard.48 During plant decomposition, the glucosinolates are hydrolysed and various toxic compounds are released. The best-known and highly active compounds are isothiocyanate derivatives (ITC). The particular glucosinolates produced are characteristic for the plant species. For example, Brassica napus primarily has non-ITC-releasing glucosinolates, while Indian mustard, B. juncea, mostly has ITC-releasing glucosinolates.34 This species has been effective in reducing populations of Ralstonia solanacearum and various nematodes (Meloidogyne chitwoodi, Tylenchus semipenetrans) and fungi (Sclerotinia minor, Rhizoctonia solani).49 Allium spp. are known to release aliphatic disulfides, including dimethyl disulfide.34,50 In practice, Allium spp. are not often used for biofumigation, although they are used as rotation crops. Rotation with Chinese leek (A. tuberosum) can successfully suppress Panama disease (caused by F. oxysporum f. sp. cubense) on bananas. The effects are related to direct effects on spore germination and survival, which can be considered as a biofumigation effect.51 Besides Brassica and Allium species, plants in many other genera have been reported to have biofumigation properties, e.g. certain members of the Boraginaceae, owing to their pyrrolizidine alkaloid contents.52,53 The effectiveness of biofumigation with green manures is affected by crop species and cultivar, the amount of biomass produced, crop age at the time of incorporation, its moisture content, the size of fragments and the depth and distribution after incorporation into soil.54 For biofumigation with brassicas, care has to be taken that the plants are incorporated into the soil shortly before flowering when the glucosinolate contents are highest.54 In addition, factors that favor glucosinolate hydrolysis, www.soci.org www.soci.org A HC van Bruggen, A Gamliel, M R Finckh Table 2. Tomato corky root (Pyrenochaeta lycopersici) severity (percentage total root length with brown transversal bands) in conventional and organic farming systems in a greenhouse experiment in Wageningen, the Netherlands, and in a field experiment in Davis, California (van Bruggen AHC et al., accepted for publication)13,191 Conventional Location Rotation Greenhouse Greenhouse Field Field Field Field Field Field Field Field Noned None Two-yeare Two-year Two-year Two-year Four-yearf Four-year Four-year Four-year Organic Yeara Meanb Stderc 2 3 6 7 8 9 6 7 8 9 68.15 57.67 49.83 11.23 22.10 31.67 3.47 3.03 5.03 16.67 2.75 3.00 3.55 2.73 1.55 8.43 0.72 1.67 0.75 3.33 Mean 50.67 54.00 2.30 2.70 2.43 8.33 2.30 2.70 2.43 8.33 Stder Significance 4.10 2.89 0.80 0.67 0.43 1.67 0.80 0.67 0.43 1.67 <0.05 – <0.01 <0.01 <0.01 <0.01 – – 0.05 <0.01 a Number of years after initiation of the experiment. b Mean severities of four blocks. c Standard error of the mean. d Tomatoes were grown continuously in this experiment; in commercial organic greenhouse production a three-year rotation is required. e Two-year rotation in the conventional system (tomato–wheat); four-year rotation in the organic system (tomato–safflower–bean–corn plus winter cover crops). f Four-year rotation in the conventional system (tomato–safflower–wheat/bean–corn); the same organic plots as in the comparison with the two-year conventional system. seeds against pathogens. The effectiveness of these products is frequently not as good as that of synthetic fungicides, but they are important in organic plant production, as they frequently have plant-growth-promoting characteristics.70 Vegetatively propagated plants, such as potatoes, strawberries and flower bulbs, must also start with certified, clean planting materials.71 Organic potato production from organically produced ‘seed’ is frequently affected by black scurf (Rhizoctonia solani) during emergence, and the quality of the product can be reduced by visible sclerotia.59 Production of healthy, certified seed potatoes is therefore essential. Interestingly, some organic growers have fewer problems with black scurf if they use seed tubers produced on their own farm as opposed to organic certified seed tubers produced elsewhere. There seems to be a Rhizoctonia decline phenomenon at certain organic arable farms.72 Certified seed potatoes also need to be free from Phytophthora infestans, as late blight constitutes an even greater problem in OF than in CF.73 – 76 34 2.2.2 Temporal isolation Crop rotation, avoidance of early-season planting of warm-season crops and avoidance of late-season planting of cool-season crops are means of temporal isolation of the pathogen as a management tool. Also, planting times can be adjusted to avoid heavy aphid flights or periods when other diseases are known to surge.77 For example, organic growers in temperate regions avoid severe damage from late blight by planting early-maturing presprouted potato varieties early in the growing season, so that tubers have grown to a reasonable size by the time late blight becomes pervasive.13,75,78 Crop rotation prevents inoculum build-up over the years and allows the natural decline of various pathogens (Table 2).17 Crop rotations are usually longer in OF than in CF: in Europe, about 7 and 3 years for organic and conventional field crops respectively. The rotation in OF may include a multiyear grass or grass/legume ley or alfalfa crop contributing to the formation and maintenance of a wileyonlinelibrary.com/journal/ps healthy soil.7,17 It may also include winter cover crops for nitrogen fixation or a reduction in nitrate leaching.79 The choice of the cover crop is important to reduce the chance of disease outbreaks and nematode damage in the following cash crop.5,19,20 Cover crop mixtures usually perform better than single species owing to optimal niche utilization and reduced spread of diseases and pests.80 Some cover crops are planted as trap or allelopathic crops for nematodes. The first to identify and develop a successful trap crop using brassica varieties against sugar beet cyst nematodes (Heterodera schachtii) was Julius Kühn in 1858.81 However, the brassica plants need to be carefully managed as they will enable multiplication of the nematodes if not killed in time. Trap crops that can attract nematodes but do not allow their reproduction are even more attractive. For example, Crotolaria spp., Mucuna spp., Tagetes spp. and some brassicas can be used in a crop rotation for this purpose.49 Marigolds (Tagetes spp.) are effective in controlling polyphagous nematodes such as Pratylenchus or Meloidogyne spp., even though not all marigold species are equally effective for all nematodes in all soils.52 Although crop rotation is an effective approach, it has a limited effect on disease development if the pathogen is carried over long distances by wind.82 In addition, pathogens with a wide host range and persistent overwintering structures, such as Sclerotinia sclerotiorum, are difficult to control by crop rotation, unless cereals and grasses take a prominent place in the rotation. Diseases such as white mold can therefore be really problematic on organic farms that specialize in vegetable production or have a too short rotation.80 For certain Fusarium species, the host range is so wide (e.g. F. avenaceum) that only comprehensive soil health management will help to avoid problems.17,83 Overall, the limited problems with root diseases on organic farms can be attributed largely to the longer rotations in OF than in CF. 2.2.3 Spatial isolation Spatial isolation refers to separation of the pathogen from a susceptible host plant or a population of susceptible host plants. It can © 2015 Society of Chemical Industry Pest Manag Sci 2016; 72: 30–44 Plant disease management in organic farming systems be divided into horizontal isolation (separation of fields by natural vegetation or wind breaks) and vertical isolation,84 for example by deep plowing of infected plant residues.85,86 Horizontal isolation is more common in OF than in CF, especially by natural field margins, and will be discussed in more detail in Section 2.3.4.6,85 Deep plowing can remove inoculum out of reach of a susceptible crop. For example, white mold (Sclerotinia sclerotiorum) of various dicotyledonous plants can be controlled by burying the sclerotia. However, repeated deep plowing can bring the sclerotia back to the surface, possibly resulting in severe infection in later years, because sclerotia may not decay in deeper soil layers low in microbial activity.86 For ecological reasons, deep plowing should preferentially be avoided. Shallow tillage is preferred in OF in order to eliminate weeds and create a seedbed for the new crop. 2.2.4 Vector control Viruliferous vectors can be prevented from probing by the use of straw or plastic mulches or oils that repel aphids.87,88 Straw mulch is effective in reducing potato virus Y infections because the texture of the straw seems to confuse the aphids.89 The most effective plastic mulches are those based on aluminum reflecting a maximum of daylight, including UV. These films cause disorientation of aphids and whiteflies and reduce their approach to the crop.90 Reflective yellow mulches are widely used in open field production in the summer in arid areas in Israel.91 The mulch attracts whiteflies onto the hot film, resulting in their mortality. However, this effect lasts only for the first growth period until the full canopy is developed. Yellow plastic mulches were not effective in Florida, probably because of climatic differences.92 In greenhouse production, good protection of crops against aphids and whiteflies can be achieved by covering the structure with UV-absorbent film combined with insect-proof nets.93 Apparently, the reduced level of UV light causes confusion in the insects, which need UV light for navigation. Natural enemies will help to keep aphid or whitefly populations in check but will be less effective in very warm weather when aphids reproduce rapidly. Moreover, a reduction in aphid or whitefly populations will be insufficient to control virus diseases, in particular non- and semi-persistent viruses.94 Nevertheless, the application of approved pesticides to prevent vectors is also common on organic farms, as described in Section 2.4.1. Pest Manag Sci 2016; 72: 30–44 (P. infestans) appears in isolated sections of potato fields, spread of the disease may be slowed by quickly destroying infected plants, for example with a flamer. Killing the infected but living potato tissue and all healthy plants within 5 m of the infection site halts further spore production.18,75 However, to be effective, fields have to be scouted almost daily to catch early infections, making this method unlikely to succeed in general. For the control of many other diseases, OF resorts to the maintenance of soil and ecosystem health. 2.3.1 The soil environment As a result of various organic amendments and a great variety of crops, including cover crops, soil quality is generally better in OF than in CF. In particular, water penetration and holding capacities are frequently better in organic than in conventional soils.10 Consequently, drought stress is less prevalent and yields can be higher in OF compared with CF in years with insufficient precipitation.97 The ability of the soil to provide the right amount of water is one of the most important soil physical factors influencing plant health. In compacted soil with local flooding, water molds such as Pythium, Phytophthora and Aphanomyces are triggered to produce zoospores that swim towards and infect host roots under wet conditions.98 Higher aggregate stability in organic systems significantly reduced tomato root rot, caused by Phytophthora parasitica, compared with conventional systems.13 Improved porosity by earthworms (Lumbricus terrestris) resulted in a reduction in Verticillium and Fusarium wilt on various fruit and vegetable crops and cereal foot diseases.99 – 101 Drought stress can be partially alleviated by irrigation. However, flood irrigation may result in greater susceptibility to root diseases and increased pathogen spread compared with drip irrigation. For example, lettuce corky root (Rhizorhapis suberifaciens) and drop (Sclerotinia minor) are enhanced by furrow irrigation but reduced by drip irrigation.102 – 104 Also, the spread of Phytophthora root rot of pepper (P. capsici) is enhanced by furrow irrigation.105 Improved soil quality in OF is also expressed in the soil chemical environment. On long-term organic farms, where stable organic matter has built up in the soil, nitrate concentrations are generally lower than in conventionally managed soils. Soil and plant nitrogen concentrations can have a profound effect on plant disease severity.8,9,18,106 High nitrogen concentrations in soil and plant tissues, in particular nitrate, may predispose a crop to several root rotting or wilt pathogens such as Fusarium spp., as well as to biotrophic foliar pathogens such as those causing powdery mildew and rusts and some necrotrophic pathogens such as those causing rice blast and leafspots on wheat.7,9,23,107 – 109 Similarly, several bacterial diseases are promoted by high nitrogen levels.103,104,110 Plants high in nitrogen also support large aphid, leafhopper or planthopper populations, potentially resulting in increased virus transmission.13,77,111 Soluble phosphorus contents are generally lower in OF than in CF, where phosphorus fertilizers are applied. Organic farmers can replenish phosphorus by application of rock phosphate, which releases phosphorus only slowly, or by fertilization with animal manures, especially from monogastric animals, that are rich in phosphorus. In soils low in available phosphorus, arbuscular mycorrhizal fungi (AMF) colonize plant roots more extensively, potentially protecting the plants against pathogenic root-infecting fungi.7,112,113 However, AMF are seriously affected by plowing.114 Shortages of some elements may enhance susceptibility to certain diseases, for example potassium shortages increase the © 2015 Society of Chemical Industry wileyonlinelibrary.com/journal/ps 35 2.3 Regulation of establishment of pathogens in organic crops Once a pathogen has entered a crop field, various conditions can either enhance or suppress its infection, multiplication, spread and thus establishment in the field.83,95 These conditions include environmental conduciveness, host quality and resistance, including resistance diversity, the presence of suppressive agents in the community that regulate epidemic development or a combination of these factors.13 In addition, physical impedance to spread by enhanced distances or physical barriers between hosts can contribute to vector and pathogen regulation. Natural disease control can be accomplished by increasing the diversity in the terrestrial and soil food webs in the agroecosystem, for example by enhanced vegetation diversity and a variety of recalcitrant organic amendments.4,7,12,96 When detected early, disease spread might be slowed somewhat by removing and destroying infected plants or plant parts while taking care not to transport the disease by hand or on infected tools and equipment to healthy plants. When late blight www.soci.org www.soci.org risk of Verticillium wilt in cotton, and calcium shortages enhance susceptibility to Pythium root rot.9,23 Calcium is usually not in short supply in organic soils owing to the organic amendments and relatively high pH, but potassium availability can become critical on organic farms unless it is replenished by potassium in manure or potassium–magnesium sulfate rock.112 Especially important in this context are also the balances among nutrients, e.g. Ca/Mg.9,23 The addition of organic substrate will enhance the activity of primary decomposers, mainly bacteria and fungi, and the associated food web, in particular bacteria-feeding protozoa and nematodes and fungivorous collembola, mites and nematodes.5,112,115 – 119 Primary decomposers can act as antagonists of plant pathogens by competition for nutrients, antibiosis and parasitism, while the micro- and mesofauna can contribute to control of plant pathogens by predation.7,118 For example, suppression of damping-off by Pythium and Rhizoctonia species 1 week after the application of fish emulsion was attributed to microbial activity.115,116,120 Furthermore, earthworm populations can be enhanced by organic amendments and contribute to improved soil structure. The combination of improved soil structure, increased microbial activity and the long-term build-up of antagonists appeared to be responsible for a reduction in Rhizoctonia bare patch disease on wheat over time.28,29 In addition to increased microbial and faunal activity, enhanced biodiversity has been associated with root disease suppression.7,9 Organically managed soils generally have a greater microbial and faunal diversity and evenness than conventionally managed soils.10,117 This may increase the chance of the presence of specific antagonists or predators. Higher diversity of non-pathogenic strains of particular pathogenic fungi or bacteria has also been documented.7,121 These non-pathogenic strains are thought to be responsible for the suppression of pathogens of the same genus or species.122 In addition, complex evolutionary dynamics after organic amendments may play a role.116,123 Over time, the selection of specific antagonists, such as Streptomyces species, may become more prevalent in particular crop rotations. The actual mechanism involved in disease suppression may vary according to the type of organic matter applied, the pathogen present and the environmental conditions. No matter by which mechanism, regular additions of hard-to-decompose organic amendments, such as plant residues high in lignin and cellulose, mature green waste compost or composted animal manure, to soil generally enhance disease suppression.14,22,96,124 – 126 36 2.3.2 The aerial environment Many foliar diseases are enhanced by moist or humid conditions. Organic management aims to provide air and light and to reduce relative humidity by thinning, pruning, leaf plucking, removing weeds, using a wider planting distance, planting parallel to the wind direction or ventilating the greenhouse.24,85 Leaf removal in grape vineyards is a common practice to control diseases such as Botrytis rot and powdery mildew on grapevines in both organic and conventional vineyards.26,127 On the other hand, organic arable crop growers sometimes attempt to suppress weeds and increase yields by creating a dense, quickly closing canopy by narrow row spacing and high seeding rates. Unfortunately, this results in a microclimate that is highly suitable for the development of various foliar diseases. Low-growing living mulches between crop plants may be a better option.128 In addition, excessive fertilization with easily available nitrogen sources such as animal slurries at planting time will create dense canopies of luxurious, relatively weak foliage that is highly susceptible to wileyonlinelibrary.com/journal/ps A HC van Bruggen, A Gamliel, M R Finckh various diseases, enhanced by a humid microclimate. Such a situation would be highly conducive for late blight development.129,130 Diseases such as late blight and downy mildew can best be managed by selecting growing sites with good air circulation, full sunlight and low humidity, without excess nitrogen, especially if resistant varieties are not available.131 In addition, mulching the soil in greenhouses for the production of tomatoes and cucumbers can reduce the severity of late blight and downy mildew.132 Finally, the greenhouse temperature can be increased so much, for example by solar heating, that the oomycete causing downy mildew of basil can be killed while the plants survive.133 The choice of irrigation method also affects the microclimate.102,134 Sprinkler irrigation can enhance dispersal of pathogens and increase the leaf wetness period and the humidity in crops, increasing the chance of infection and spread by foliar pathogens. This holds especially for bacterial pathogens and fungal pathogens that are splash dispersed. The timing of irrigation can be adjusted to prevent extended leaf wetness periods and disease outbreaks.135 Moreover, the use of drip irrigation will also reduce the incidence and severity of both foliar and root pathogens.102 In spite of its benefits, drip irrigation is not more common in OF than in CR. Standing water may have a different effect on disease development, however, as it may increase temperatures at night and reduce them during the day, reducing leaf wetness overall, although soil-borne pathogens may become problematic. 2.3.3 Plant resistance The use of cultivars resistant to diseases, insect vectors and nematodes is at least as critical to successful OF as it is for CF. Many organic farmers prefer open pollinated cultivars to hybrids, even if the former are more susceptible to certain diseases, because open pollinated varieties generally have more genetic variation than hybrids. However, when diseases can severely limit crop yield, organic farmers try to use the most resistant varieties available to them. For example, organic growers generally avoid potato cultivars that are extremely susceptible to late blight. Instead, they choose cultivars that have more general resistance to this disease and mature early to avoid epidemic development.75,136 Similarly, it is very important to organic producers of perennial crops such as apples to select cultivars with broad resistance to the main pathogens.137 For several of the most damaging plant diseases, such as tomato late blight and white rot (Sclerotium cepivorum) of Allium species, no horticulturally acceptable resistant cultivars are available. However, intensive screening efforts are under way to find potato cultivars with broad resistance to late blight.136 Commercial seed companies rarely invest in the development of resistant cultivars for specialty or minor vegetable crops. Moreover, a cultivar that is resistant to one disease may be quite susceptible to another. Yet there are also vegetable crops with resistance to multiple diseases. Some plant selections may have excellent resistance to soil-borne pathogens and nematodes but be horticulturally unacceptable. In that case, horticulturally desirable crop scions may be grafted on resistant rootstocks of a different species or genus in the same family.138,139 Grafted annual crops mostly belong to the Cucurbitaceae and Solanaceae with resistance to Fusarium (F. oxysporum) and Verticillium (V. dahlia) wilt, root rot by Phytophthora spp., corky root (Pyrenochaeta lycopersici), bacterial wilt (Ralstonia solanacearum) and root-knot nematodes (Meloidogyne spp.). As grafted transplants are relatively expensive, they are primarily used for intensive vegetable crops, for example in © 2015 Society of Chemical Industry Pest Manag Sci 2016; 72: 30–44 Plant disease management in organic farming systems greenhouses. On the other hand, the use of grafted fruit trees or vines on disease-resistant rootstocks is very common also in conventional orchards and vineyards, because perennial crops could not be replaced easily if they were to succumb to a disease. Examples of disease-resistant perennials grafted onto resistant rootstocks are fire-blight- or Phytophthora-resistant apple trees and aphid- and nematode-resistant grapevines.26,140 The mechanisms underlying resistance range from physical features such as a waxy epidermis to toxic secondary plant compounds.141 Some of the resistance features have a broad activity against many pests and diseases and are based on multiple genes. Other forms of resistance are specific and governed by one or a few genes, which may be overcome relatively easily by the pathogen. For example, new races of Peronospora farinosa f. sp. spinaciae, the causal agent of spinach downy mildew, periodically appeared in California, causing significant damage to the previously resistant spinach cultivars.142 However, not all single-gene resistances are equally easily overcome. Especially recessive qualitative resistances seem to be based on different mechanisms that have proven to be very stable.143,144 Prominent examples are barley mlo powdery mildew resistance, which has not yet been overcome since its introduction in 1976, the resistance in cabbage against F. oxysporum f. sp. conglutinans, which has been effective since the 1920s, and the resistance to corky root of lettuce by R. suberifaciens, which has been effective since the 1980s.129,144,145 Some forms of resistance only become effective upon induction. There are two types of induced systemic defense: systemic acquired resistance (SAR) and induced systemic resistance (ISR).18,146 The first can be induced by various pathogens, pests, chemicals and other damaging agents, and is mediated by the salicylic acid pathway. The second is mainly induced by plant-growth-promoting rhizobacteria (PGPR) or fungi and involves enhanced production of jasmonate and ethylene, which can inhibit root and foliar plant pathogens as well as some insect pests.70,146 ISR may be more common in organically managed plants, as it is strongly affected by organic amendments such as composts or chitin.16,70,125,146,147 The ability of compost to induce resistance depends on the batch of compost, the recolonization of the compost after the heating phase, the pathosystem and the soil type.126,148 Several species of PGPR, such as Bacillus spp., have been isolated that are effective at inducing resistance to particular below- and above-ground fungal pathogens and even viruses.70,94 Under some circumstances, both SAR and ISR can be induced, affecting the resistance level additively. A number of chemical compounds, such as salicylic acid, potassium phosphite (also named phosphonate), silicate, specific plant extracts and microbial metabolites, can induce resistance in plants when applied to the foliage.23,109,149,150 Almost none of these chemical products has been approved for organic production at this moment in time, except when obtained from natural sources.151 Pest Manag Sci 2016; 72: 30–44 host in a mixture may also give rise to induced defense reactions, including the production and emission of volatiles that may in turn induce a resistance response in neighboring susceptible plants.6 In spite of the potential benefits, crop mixtures are rarely used in current organic agriculture in the northern hemisphere, primarily owing to technical problems with cultivation and harvesting. An exception is the planting of mixed undercrops, which is common in organic orchards. Moreover, planting of cultivar mixtures, especially of cereal crops, has been widely adopted in some regions, and also in conventional production systems.6,107,108 Extensive research has been done on the effects of intercropping, strip cropping, crop mixtures and mosaics of crop fields to control late blight of potatoes. Resistance and species diversity in the field may counteract late blight development to some degree.75,154,155 However, this effect is not sufficient to provide protection unless combined with several other methods, and even then, if the climatic conditions are too favorable to the disease, organic farmers have little means to combat late blight effectively except for copper sprays.75 2.3.5 Enhancing and augmenting biological control Enhancing natural control is preferred over the application of biological control agents in OF. Natural control is enhanced by increasing the diversity in the terrestrial and soil food webs in the agroecosystem.4,5,7,12,96 A complex microbial community as found in organically managed soils and on plant surfaces generally contains a variety of general antagonists and parasitic microorganisms such as Pythium oligandrum or Trichoderma species that suppress pathogenic fungi. Organic farmers sometimes try to increase microbial populations and diversity on plant surfaces by applying compost extracts, also called compost teas, especially in the United States.64,96 The effects are variable, depending on the starting material, the composting and fermentation procedures and period, the water ratio, added nutrients such as molasses, temperature and pH.157 The application methods also vary and need to be optimized to enhance the effectiveness of compost teas.158 Compost extracts from manure and plant materials have sometimes been used to slow down late blight development on potatoes or tomatoes.158 – 160 Extracts from composted olive wastes were most effective in controlling tuber blight.161 However, the use of compost tea is now regulated in organic production owing to concerns about possible contamination with human and animal pathogens, especially when molasses is used to enhance microbial growth on the plant surface.162,163 Similarly, suspensions of microbial communities are sometimes mixed into compost heaps or sprayed directly onto the foliage, especially in tropical countries, with the intent to enhance microbial community diversity and increase resistance against pathogens. However, the effectiveness of these suspensions has not been sufficiently proven in refereed articles.164 The other approach to biological control is direct application of biocontrol agents, also called augmented biological control. Although many potential biocontrol agents have been identified, relatively few formulated products have been approved for disease control in organic crop production, as petroleum-based synergists or carriers cannot be used in organic formulations.151 Lists of approved ‘microbial inoculants’ and ‘microbial products’ in the United States can be found on the website of the Organic Materials Review Institute (http://www.omri.org). In the EU, biological control agents that are registered for organic agriculture can be found under Council Directive 91/414/EEC and Council Regulation (EC) No. 834/2007.165 Approved biocontrol © 2015 Society of Chemical Industry wileyonlinelibrary.com/journal/ps 37 2.3.4 Increasing crop diversity Mixing species or varieties differing in resistance to specific pathogens can curb the epidemic spread of some foliar and root diseases owing to loss of inoculum on non-host crops.6,80,129,152,153 However, the effect of diversity on epidemic development is scale dependent.84,152,154 – 156 Pathogen spread and epidemic development is primarily determined by the number and distribution of susceptible plants in the mixture or crop mosaic; the longer the distance between susceptible plants, the slower the spread.21,80 Resistant plants in a mixture form obstacles and traps to pathogens and their vectors. Incompatible combinations of pathogen and www.soci.org www.soci.org products are sometimes used as seed treatment or as soil drench in the greenhouse, for example various species of Gliocladium, Trichoderma, Streptomyces, Pseudomonas and Bacillus, primarily for the control of soil-borne plant pathogens.151 Some B. subtilis strains are used against foliar diseases, for example against Botrytis cinerea on grapevines and fire blight (Erwinia amylovora) on apples and pears.165 The yeast Aureobasidium pullulans is also used to control fire blight.140,165 Nematode populations could potentially be reduced by species of the fungal genera Myrothecium and Paecilomyces or the bacterial genera Burkholderia and Pasteuria.166 Biocontrol agents are frequently used in apple orchards.140,165 However, they are applied only occasionally in organic annual crop production, except for natural enemies of insect pests and vectors, especially in greenhouse production.24 For example, the greenhouse whitefly Trialeurodes vaporariorum has been controlled successfully by the parasitic wasp Encarsia formosa. In the field, products based on various Bacillus thuringiensis subspecies are frequently used. The mechanisms underlying successful biological control vary from niche competition, antagonism and parasitism to predation. These modes of action are more likely to control below-ground diseases and pests than aerial diseases, which are much more influenced by microclimatological conditions. When microbial products are applied on seeds or soil, they may also induce systemic resistance to diseases of above-ground parts. For example, tomatoes drenched with a suspension of Trichoderma harzianum or Streptomyces griseoviridis had reduced levels of early blight or gray mold, respectively, compared with the untreated control.151 A recent approach to biological disease control is through the use of endophytes, with substantial progress reported for bananas.167 However, the application of biocontrol agents is not always successful, especially when applied to field soil. This may be due to the large microbial diversity and buffering capacity of organically managed field soil.168 For example, an antibiotic-producing strain of Pseudomonas fluorescens did not survive as well in organically managed as in conventionally managed soil.169,170 It effectively controlled take-all disease (Gaeumannomyces graminis) in conventionally but not in organically managed soil. The greater biodiversity in organic agroecosystems may reduce the effectiveness of augmented biological control agents.169 38 2.4 Curative control of pathogens in organic crops Curative control techniques involve application of measures after a pathogen has established itself in the crop. There are limited options for curative control allowed in OF. In principle, the use of synthetic pesticides is prohibited in OF. If there are exceptions for restricted use, these pesticides are specifically listed. Pesticides from natural sources such as plant extracts or toxins produced by bacteria are often allowed after a thorough case-by-case evaluation, provided that no synthetic materials are used in their formulation. Mined products are usually also allowed, e.g. silicate from diatomaceous earth. In most countries, copper fungicides are considered ‘mined, natural products’ and are allowed for use against bacterial and fungal diseases, but the number of countries with restricted use of copper fungicides is increasing, especially in Northern Europe.149,171,172 Table 1 provides a representative list of fungicides and insecticides, plant products, microbial agents and other naturally available materials typically approved under organic standards. A detailed list of products allowed for organic production in the United States can be found on the website of the Organic Materials Review Institute (http://www.omri.org). For Europe there are European and national regulations that are wileyonlinelibrary.com/journal/ps A HC van Bruggen, A Gamliel, M R Finckh constantly updated online.173,174 Many organic farmers try to avoid using them except in emergency situations, because they do not like to be seen with a spray rig for fear of being unjustly accused of fraud.75,76 2.4.1 Pesticides and plant or microbial extracts Copper fungicides have been used primarily to control diseases caused by Oomycetes (downy mildews and late blight), but also other foliar diseases that are difficult to control without fungicides, such as apple scab, tomato anthracnose, various coffee diseases and black Sigatoka disease of bananas.25 – 27,74,75,165,172,175,176 However, copper is not only toxic to bacteria and fungi but also to plants, especially during periods of cool wet weather when many plant pathogens thrive.177 At recommended concentrations to control plant pathogens, copper is also toxic to various soil organisms such as earthworms and many microorganisms, even at sublethal concentrations.165,178 Repeated and excessive use of copper can lead to accumulation in soil and in the food web. Accumulation of copper in food products is toxic to humans as well. For this reason, commercial copper products are listed as ‘regulated’, meaning that the total dosage is limited to prevent the build-up of toxic levels of copper in the soil, and the use of copper is quite controversial and may be banned in the near future.75,165,179 Sulfur fungicides are widely used to control powdery mildew on various crops and scab (Venturia inaequalis) on apples and pears.27,140,165 It is applied as wettable sulfur (in the field and orchards) or finely ground sulfur dust (mostly in greenhouses and vineyards). Sulfur is generally quite effective in controlling powdery mildews, but much less effective than synthetic fungicides for control of apple scab, especially under high disease pressures.180 Wettable sulfur combined with copper hydroxide or with lime sulfur gave better control of primary scab, but resulted in more phytotoxicity than wettable sulfur alone.180 Sulfur can also be phytotoxic by itself, especially at temperatures above 30 ∘ C.151 Bicarbonate salts can also be used for disease control in organic agriculture.165 Potassium and sodium bicarbonate have been cleared by the United States Environmental Protection Agency (EPA) as exempt from residue tolerances.181 Sodium bicarbonate (baking soda) is allowed for the control of various diseases by most regulatory agencies, but is not as effective as potassium or ammonium bicarbonate.151,181 Bicarbonates are effective primarily against powdery mildews, apple scab and necrotic leaf spot diseases.181 The effectiveness of bicarbonates can be enhanced by an approved spreader-sticker like soap or oil.151,182 Oils are not only used as spreader-stickers but can also control some fungal diseases and hurt or repel insects. Some mineral oils, vegetable oils and fish oils are permitted for use in organic agriculture.151 Mineral and plant-derived oils are particularly effective against powdery mildews, and may enhance host plant resistance.183 Oils can also inhibit insect vectors by interfering with the gas exchange, degrading tissues or altering the behavior of the insects. Some oils inhibit the ability of aphids to acquire and transmit viruses.184 Moreover, insecticidal soaps (potassium and ammonium salts of fatty acids) can be used as surfactants combined with (natural) pesticides, and can also have direct effects on soft-bodied insects such as aphids and whiteflies by disrupting the cuticle layer.151 The effects on plant diseases such as powdery mildews are quite variable.151 As their name suggests, insecticidal soaps have been registered for insect control in organic agriculture, but most of them have not been approved yet for use against plant-pathogenic fungi, except coconut soap.140,165 © 2015 Society of Chemical Industry Pest Manag Sci 2016; 72: 30–44 Plant disease management in organic farming systems Extracts from several plant species can be toxic to a variety of plant pathogens and insect vectors. The extracts are obtained by water extraction or various solvents. Several plant extracts are allowed under organic guidelines, provided that they are not formulated in petroleum-based synergists or carriers (http://www.omri.org). For example, yucca and citrus extracts are listed as commercial products for organic agriculture. However, it is difficult to find scientific evidence for the effectiveness of most plant extracts. For example, horsetail (Equisetum) extracts have been applied to control diseases such as peach leaf curl and powdery mildew, but the results may be variable. One of the active ingredients could be silicate, because horsetails contain relatively high concentrations of silicate in the foliage.9 Similarly, home-made extracts from horseradish roots (Armoracia rusticana), from dock (Rumex sp.) and from nettle (Urtica sp.) have been used to control various necrotic leaf spot diseases and downy and/or powdery mildews.147 Both horseradish roots and dock are well known for their antioxidant properties. Extracts from chives and garlic have also been tested against various fungal and Oomycete diseases. Allium species emit a volatile compound, allicin, that has fungicidal properties.159,185 Extracts from many herbs, spices and medicinal plants are being tested for their effects on various plant diseases.172 For example, a formulated and available plant-based fungicide is the organic pesticide Tillecur® based on mustard extracts, which successfully reduces stinking smut (Tilletia caries) when applied as seed treatment on wheat.65 However, only a few products have been approved by organic regulatory agencies, for example lecithin, which is extracted from soybeans and is effective against various powdery mildews.165 Several microbial extracts can promote induced resistance, for example cell wall fragments of Penicillum chrysogenum (PEN).150,186 PEN is active against a wide spectrum of pathogens affecting a number of host species as it contains one or more of the substances, or substance groups, that trigger the metabolic processes typical of induced resistance. In addition, an extract from brown algae or kelp, laminarin, has been approved for use in the EU.174 Kelp extracts are also on the OMRI list. These extracts could become an excellent alternative to copper fungicides in organic agriculture.150,186,187 In spite of the fact that some of the plant and microbial extracts may be effective compared with untreated control plants, the extracts are often less effective than synthetic fungicides. Therefore, an integrated approach to plant disease management, including optimal cultural practices, is even more necessary in OF than in CF systems.7,15 Pest Manag Sci 2016; 72: 30–44 pests.61 Similarly, dusting of fine sulfur particles for the control of powdery mildew and mites has been widely used in organic greenhouses and orchards.24,171 Such application techniques result in a high and uniform spray deposit on both the upper and under sides of leaves, enhancing the probability of effective control. 3 CONCLUSIONS AND RECOMMENDATIONS CF systems are typically maintained by continuous external inputs to provide nutrients and keep pests and diseases under control. Organic farmers strive for a healthy ecosystem with high biological diversity, minimal nutrient losses and natural buffering capacity against diseases and pests.9,12,95 However, it takes many years for new microbial and chemical equilibria with relative stability to become established after the conversion from CF to OF, and during the transition period, several pest and disease outbreaks may occur.188,189 Nevertheless, epidemic spread of many plant diseases can be curbed as a result of greater crop diversity in time and space and the use of natural vegetation, barrier and cover crops. After a transition period of about 5 years, soil-borne diseases are commonly suppressed in OF, including fungus- and nematode-transmitted virus diseases, provided crop rotation is sufficiently long.8 Shoot diseases are either more or less severe in OF than in CF, depending on the particular pathosystem and climatological circumstances.15 Diseases that are promoted by high nitrogen contents in plant tissues, such as some rusts and powdery mildews, are usually not problematic in OF.13,111 However, foliar pathogens that survive in crop residues or on weeds can be enhanced in OF, depending on the level of natural control achieved. Insect-vector-transmitted virus diseases can also be more problematic in OF owing to the smaller scale and thus the proximity of field margins containing alternative hosts and virus vectors, although reduced nitrogen availability may curb virus vector activity.77 In addition, diseases caused by multiple-cycle pathogens for which no adequate resistance is available, such as late blight of potatoes, can constitute a severe problem for organic farmers in humid areas, as effective control measures do not exist.165 Lack of resistances represents a major problem in many minor crops. To overcome this, concerted breeding efforts for OF will be required, with the involvement and participation of organic farmers.190 Many of these plant disease problems cannot be solved in short-term small-scale controlled experiments but need to be addressed at a higher integration level, especially considering long-term effects of soil management. Even more than conventional farmers, organic farmers need to reach various objectives with a coherent set of cultural practices.17,71 Optimal farming systems will need to be designed that satisfy the requirements of sustained profitability, regional self-reliance, crop and ecosystem health and minimal environmental impact. To this end, existing and desirable farming systems can be analyzed and redeveloped using crop growth, nutrient cycling and farm management models.17 This kind of research requires a systems approach in which scientists from various disciplines work together. Strategic decisions that are geared towards minimization of pest and disease outbreaks and long-term sustainability could include regional deployment of crops, optimal rotations and integration of semi-natural and agricultural areas in the region and on the farm. In addition, organic regulatory agencies need to revise certain decisions with respect to the materials that are allowed for disease control. For example, there is no scientific reason why sodium bicarbonate would be allowed while the more effective © 2015 Society of Chemical Industry wileyonlinelibrary.com/journal/ps 39 2.4.2 Pesticide application Effective spraying technology must take into account the nature of the active agent: biocontrol microorganisms or their metabolites, plant extracts or fungicides. Biocontrol agents must be kept alive, and need to be formulated and applied with special care. Storage and application of microbial metabolites, plant extracts and fungicides should abide by the same principles governing the application of conventional pesticides in order to accomplish pest control. Unlike synthetic pesticides with systemic capacity, the above-listed pesticides have limited mobility. Hence, optimal coverage of the target plant organs is needed for their effective performance. Equipment that produces fine droplet sizes dispersed in air can effectively deliver the spray to all target surfaces, and the use of aerosols has been effective at controlling a wide spectrum of www.soci.org www.soci.org potassium bicarbonate is not cleared for use by many certification agencies, although both salts are equally innocuous for the environment. However, a full risk assessment would be needed. Another example is the acceptance of copper as a fungicide for OF. The negative environmental side effects have been demonstrated in many scientific publications, but the historical use of copper in Bordeaux Mixture to control downy mildew of grapes before the large-scale introduction of synthetic organic fungicides seems to provide a precedent for copper use in organic crop production.172 As the demand for organic products continues to grow, so too will the need for improved production systems to fill this demand. Increasingly, organic production takes place on small-scale farms in developing countries, often under conditions of high environmental stress. Nevertheless, owing to improved soil quality and greater water use efficiency, OF can be more productive under those circumstances than CF with limited synthetic inputs.97 OF can thus contribute significantly to providing food security. However, more research is needed to optimize OF under those conditions minimizing pest and disease outbreaks. A concerted interdisciplinary effort will be required to attain these goals. The recent book Plant Diseases and their Management in Organic Agriculture contributes to this effort by devoting several chapters to the production of organic food crops in the tropics.76 ACKNOWLEDGEMENTS We would like to thank all coauthors of the book Plant Diseases and their Management in Organic Agriculture, who indirectly contributed to this review. 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